Behavioral response of root-knot nematode, Meloidogyne incognita, to tomato, Solanum lycopersicon, root exudates

Abstract

Root-Knot Nematodes (RKNs) are major economically important group of plant parasitic nematodes distributed worldwide. RKNs cause over $100 billion yield losses annually on major crops. The damage caused to crops is due to plant root invasion by motile second stage juveniles (J2s). The J2s induce redifferentiation of the plant root cells into specialized feeding cells essential for nematode development. The hyperplasia and hypertrophy of cells surrounding the feeding cells lead to formation of typical root galls affecting transport of photosynthates from source to sink, and uptake of water and nutrients. Upon hatching from the eggs in the soil, J2s must successfully locate a host plant to invade and infect for them to survive and complete their life cycle. However, there is limited knowledge on what directs the J2s to their hosts. It is demonstrated that olfaction plays an important role in the nematode host-seeking process by following a chemical trail toward host-associated odors. The known attractants include volatile and non-volatile (water-soluble) compounds released by plant roots into the rhizosphere. The former mediates long distance attraction while the latter is involved in short distance attraction. The major source of these chemicals is root exudates from which several stimuli responses that include attraction, repulsion and aggregation have been postulated. In this study, the responses of the motile stage second stage juveniles (J2s) of Meloidogyne incognita to tomato root exudates and the non-volatile components identified in the root exudates were investigated. Using stylet thrusting, chemotaxis assays, and chemical analysis, specific metabolites in the tomato root exudates that either attract or repel J2s were identified. Ultra-Performance Liquid chromatography quadrupole time-of-flight mass spectrometry (UPLC-QToF-MS) analysis of bioactive fractions obtained from the root exudate revealed a high diversity of compounds. Five of these were identified as the phytohormone zeatin (cytokinin), the flavonoids quercetin and luteolin, and the alkaloids solasodine and tomatidine. In stylet thrusting and chemotaxis assays, the five compounds elicited concentration-dependent responses in J2s relative to 2% dimethyl sulfoxide (negative control) and methyl salicylate (positive control). Zeatin being attractive to J2s in all the concentrations and quercetin being attractive at lower concentrations and deterrence at high concentrations tested. These results indicate that J2 parasitism is influenced by root exudate chemistry and concentrations of specific compounds. Identification of zeatin and quercetin as an attractant of RKNs J2s improves our understanding of root knot nematodes chemical ecology, and that they could be used as a potential component in the IPM of root knot nematodes.